Association between Parkinson's disease and the faecal eukaryotic microbiota.
Journal
NPJ Parkinson's disease
ISSN: 2373-8057
Titre abrégé: NPJ Parkinsons Dis
Pays: United States
ID NLM: 101675390
Informations de publication
Date de publication:
18 Nov 2021
18 Nov 2021
Historique:
received:
03
02
2021
accepted:
21
10
2021
entrez:
19
11
2021
pubmed:
20
11
2021
medline:
20
11
2021
Statut:
epublish
Résumé
Parkinson's disease (PD) is one of the most common neurodegenerative disease, and is so far not considered curable. PD patients suffer from several motor and non-motor symptoms, including gastrointestinal dysfunctions and alterations of the enteric nervous system. Constipation and additional intestinal affections can precede the classical motor symptoms by several years. Recently, we reported effects of PD and related medications on the faecal bacterial community of 34 German PD patients and 25 age-matched controls. Here, we used the same collective and analysed the V6 and V7 hypervariable region of PCR-amplified, eukaryotic 18S rRNA genes using an Illumina MiSeq platform. In all, 53% (18) of the PD samples and 72% (18) of the control samples yielded sufficient amplicons for downstream community analyses. The PD samples showed a significantly lower alpha and a different beta eukaryotic diversity than the controls. Most strikingly, we observed a significantly higher relative abundance of sequence affiliated with the Geotrichum genus in the PD samples (39.7%), when compared to the control samples (0.05%). In addition, we observed lower relative abundances of sequences affiliated with Aspergillus/Penicillium, Charophyta/Linum, unidentified Opisthokonta and three genera of minor abundant zooflagellates in the PD samples. Our data add knowledge to the small body of data about the eukaryotic microbiota of PD patients and suggest a potential association of certain gut eukaryotes and PD.
Identifiants
pubmed: 34795317
doi: 10.1038/s41531-021-00244-0
pii: 10.1038/s41531-021-00244-0
pmc: PMC8602383
doi:
Types de publication
Journal Article
Langues
eng
Pagination
101Subventions
Organisme : Bundesministerium für Bildung und Forschung (Federal Ministry of Education and Research)
ID : 03FH036PB5
Organisme : Bundesministerium für Bildung und Forschung (Federal Ministry of Education and Research)
ID : 03FH036PB5
Informations de copyright
© 2021. The Author(s).
Références
Perez-Pardo, P. et al. The gut-brain axis in Parkinson’s disease: possibilities for food-based therapies. Eur. J. Pharmacol. 817, 86–95 (2017).
pubmed: 28549787
doi: 10.1016/j.ejphar.2017.05.042
Savica, R. et al. Medical records documentation of constipation preceding Parkinson disease: a case-control study. Neurology 73, 1752–1758 (2009).
pubmed: 19933976
pmcid: 2788809
doi: 10.1212/WNL.0b013e3181c34af5
Fasano, A. et al. The role of small intestinal bacterial overgrowth in Parkinson’s disease. Mov. Disord. 28, 1241–1249 (2013).
pubmed: 23712625
doi: 10.1002/mds.25522
Jost, W. H. Gastrointestinal dysfunction in Parkinson’s disease. J. Neurol. Sci. 289, 69–73 (2010).
pubmed: 19717168
doi: 10.1016/j.jns.2009.08.020
Pfeiffer, R. F. Gastrointestinal dysfunction in Parkinson’s disease. Parkinsonism Relat. Disord. 17, 10–15 (2011).
pubmed: 20829091
doi: 10.1016/j.parkreldis.2010.08.003
Cersosimo, M. G. & Benarroch, E. E. Pathological correlates of gastrointestinal dysfunction in Parkinson’s disease. Neurobiol. Dis. 46, 559–564 (2012).
pubmed: 22048068
doi: 10.1016/j.nbd.2011.10.014
Chen, H. et al. Meta-analyses on prevalence of selected Parkinson’s nonmotor symptoms before and after diagnosis. Transl. Neurodegener. 4, 1 (2015).
pubmed: 25671103
pmcid: 4322463
doi: 10.1186/2047-9158-4-1
Abbott, R. D. et al. Frequency of bowel movements and the future risk of Parkinson’s disease. Neurology 57, 456–462 (2001).
pubmed: 11502913
doi: 10.1212/WNL.57.3.456
Gao, X., Chen, H., Schwarzschild, M. A. & Ascherio, A. A prospective study of bowel movement frequency and risk of Parkinson’s disease. Am. J. Epidemiol. 174, 546–551 (2011).
pubmed: 21719744
pmcid: 3202149
doi: 10.1093/aje/kwr119
Hawkes, C. H., Del Tredici, K. & Braak, H. Parkinson’s disease: a dual-hit hypothesis. Neuropathol. Appl. Neurobiol. 33, 599–614 (2007).
pubmed: 17961138
pmcid: 7194308
doi: 10.1111/j.1365-2990.2007.00874.x
Horsager, J. et al. Brain-first versus body-first Parkinson’s disease: a multimodal imaging case-control study. Brain 143, 3077–3088 (2020).
pubmed: 32830221
doi: 10.1093/brain/awaa238
Cryan, J. F. & Dinan, T. G. Mind-altering microorganisms: the impact of the gut microbiota on brain and behaviour. Nat. Rev. Neurosci. 13, 701–712 (2012).
pubmed: 22968153
doi: 10.1038/nrn3346
Braak, H. & Del Tredici, K. Neuropathological staging of brain pathology in sporadic Parkinson’s disease: separating the wheat from the Chaff. J. Parkinsons Dis. 7, S71–S85 (2017).
pubmed: 28282810
pmcid: 5345633
doi: 10.3233/JPD-179001
Pan-Montojo, F. et al. Progression of Parkinson’s disease pathology is reproduced by intragastric administration of rotenone in mice. PLoS ONE 5, e8762 (2010).
pubmed: 20098733
pmcid: 2808242
doi: 10.1371/journal.pone.0008762
Pan-Montojo, F. et al. Environmental toxins trigger PD-like progression via increased alpha-synuclein release from enteric neurons in mice. Sci. Rep. 2, 898 (2012).
pubmed: 23205266
pmcid: 3510466
doi: 10.1038/srep00898
Zhao, Y. & Yu, Y.-B. Intestinal microbiota and chronic constipation. Springerplus 5, 1130 (2016).
pubmed: 27478747
pmcid: 4951383
doi: 10.1186/s40064-016-2821-1
Sampson, T. R. et al. Gut microbiota regulate motor deficits and neuroinflammation in a model of Parkinson’s disease. Cell 167, 1469–1480.e12 (2016).
pubmed: 27912057
pmcid: 5718049
doi: 10.1016/j.cell.2016.11.018
Choi, J. G. et al. Oral administration of Proteus mirabilis damages dopaminergic neurons and motor functions in mice. Sci. Rep. 8, 1275 (2018).
pubmed: 29352191
pmcid: 5775305
doi: 10.1038/s41598-018-19646-x
Sun, M.-F. et al. Neuroprotective effects of fecal microbiota transplantation on MPTP-induced Parkinson’s disease mice: gut microbiota, glial reaction and TLR4/TNF-α signaling pathway. Brain Behav. Immun. 70, 48–60 (2018).
pubmed: 29471030
doi: 10.1016/j.bbi.2018.02.005
Weis, S. et al. Effect of Parkinson’s disease and related medications on the composition of the fecal bacterial microbiota. NPJ Parkinsons Dis. 5, 28 (2019).
pubmed: 31815177
pmcid: 6884491
doi: 10.1038/s41531-019-0100-x
Keshavarzian, A. et al. Colonic bacterial composition in Parkinson’s disease. Mov. Disord. 30, 1351–1360 (2015).
pubmed: 26179554
doi: 10.1002/mds.26307
Forsyth, C. B. et al. Increased intestinal permeability correlates with sigmoid mucosa alpha-synuclein staining and endotoxin exposure markers in early Parkinson’s disease. PLoS ONE 6, e28032 (2011).
pubmed: 22145021
pmcid: 3228722
doi: 10.1371/journal.pone.0028032
Schwiertz, A. et al. Fecal markers of intestinal inflammation and intestinal permeability are elevated in Parkinson’s disease. Parkinsonism Relat. Disord., https://doi.org/10.1016/j.parkreldis.2018.02.022 (2018).
Romano, S. et al. Meta-analysis of the Parkinson’s disease gut microbiome suggests alterations linked to intestinal inflammation. NPJ Parkinsons Dis. 7, 27 (2021).
pubmed: 33692356
pmcid: 7946946
doi: 10.1038/s41531-021-00156-z
Wallen, Z. D. et al. Characterizing dysbiosis of gut microbiome in PD: evidence for overabundance of opportunistic pathogens. NPJ Parkinsons Dis. 6, 11 (2020).
pubmed: 32566740
pmcid: 7293233
doi: 10.1038/s41531-020-0112-6
Tetz, G., Brown, S. M., Hao, Y. & Tetz, V. Parkinson’s disease and bacteriophages as its overlooked contributors. Sci. Rep. 8, 10812 (2018).
pubmed: 30018338
pmcid: 6050259
doi: 10.1038/s41598-018-29173-4
Nash, A. K. et al. The gut mycobiome of the Human Microbiome Project healthy cohort. Microbiome 5, 153 (2017).
pubmed: 29178920
pmcid: 5702186
doi: 10.1186/s40168-017-0373-4
Schulze, J. & Sonnenborn, U. Yeasts in the gut: from commensals to infectious agents. Dtsch. Ärzteblatt Int. 106, 837–842 (2009).
Huffnagle, G. B. & Noverr, M. C. The emerging world of the fungal microbiome. Trends Microbiol. 21, 334–341 (2013).
pubmed: 23685069
pmcid: 3708484
doi: 10.1016/j.tim.2013.04.002
Enaud, R. et al. The mycobiome: a neglected component in the microbiota-gut-brain axis. Microorganisms 6, https://doi.org/10.3390/microorganisms6010022 (2018).
Gouba, N., Raoult, D. & Drancourt, M. Gut microeukaryotes during anorexia nervosa: a case report. BMC Res. Notes 7, 33 (2014).
pubmed: 24418238
pmcid: 3895777
doi: 10.1186/1756-0500-7-33
Strati, F. et al. New evidences on the altered gut microbiota in autism spectrum disorders. Microbiome 5, 24 (2017).
pubmed: 28222761
pmcid: 5320696
doi: 10.1186/s40168-017-0242-1
Unger, M. M. et al. Short chain fatty acids and gut microbiota differ between patients with Parkinson’s disease and age-matched controls. Parkinsonism Relat. Disord. 32, 66–72 (2016).
pubmed: 27591074
doi: 10.1016/j.parkreldis.2016.08.019
Kaul, A., Mandal, S., Davidov, O. & Peddada, S. D. Analysis of microbiome data in the presence of excess zeros. Front. Microbiol. 8, 2114 (2017).
pubmed: 29163406
pmcid: 5682008
doi: 10.3389/fmicb.2017.02114
Scheperjans, F. et al. Gut microbiota are related to Parkinson’s disease and clinical phenotype. Mov. Disord. 30, 350–358 (2015).
pubmed: 25476529
doi: 10.1002/mds.26069
Hopfner, F. et al. Gut microbiota in Parkinson disease in a northern German cohort. Brain Res. 1667, 41–45 (2017).
pubmed: 28506555
doi: 10.1016/j.brainres.2017.04.019
Hill-Burns, E. M. et al. Parkinson’s disease and Parkinson’s disease medications have distinct signatures of the gut microbiome. Mov. Disord. 32, 739–749 (2017).
pubmed: 28195358
pmcid: 5469442
doi: 10.1002/mds.26942
Cirstea, M. S. et al. The gut mycobiome in Parkinson’s disease. J. Parkinsons Dis., https://doi.org/10.3233/JPD-202237 (2020).
Li, W. et al. Structural changes of gut microbiota in Parkinson’s disease and its correlation with clinical features. Sci. China Life Sci. 60, 1223–1233 (2017).
pubmed: 28536926
doi: 10.1007/s11427-016-9001-4
Adiba, S., Nizak, C., van Baalen, M., Denamur, E. & Depaulis, F. From grazing resistance to pathogenesis: the coincidental evolution of virulence factors. PLoS ONE 5, e11882 (2010).
pubmed: 20711443
pmcid: 2920306
doi: 10.1371/journal.pone.0011882
Hahn, M. W. & Höfle, M. G. Grazing of protozoa and its effect on populations of aquatic bacteria. FEMS Microbiol. Ecol. 35, 113–121 (2001).
pubmed: 11295449
doi: 10.1111/j.1574-6941.2001.tb00794.x
Sun, S., Noorian, P. & McDougald, D. Dual role of mechanisms involved in resistance to predation by protozoa and virulence to humans. Front. Microbiol. 9, 1017 (2018).
pubmed: 29867902
pmcid: 5967200
doi: 10.3389/fmicb.2018.01017
Matz, C. & Kjelleberg, S. Off the hook-how bacteria survive protozoan grazing. Trends Microbiol. 13, 302–307 (2005).
pubmed: 15935676
doi: 10.1016/j.tim.2005.05.009
Hallen-Adams, H. E. & Suhr, M. J. Fungi in the healthy human gastrointestinal tract. Virulence 8, 352–358 (2017).
pubmed: 27736307
doi: 10.1080/21505594.2016.1247140
Kulas, J. et al. Pulmonary Aspergillus fumigatus infection in rats affects gastrointestinal homeostasis. Immunobiology 224, 116–123 (2019).
pubmed: 30348457
doi: 10.1016/j.imbio.2018.10.001
Dubey, M. K. et al. PR toxin—biosynthesis, genetic regulation, toxicological potential, prevention and control measures: overview and challenges. Front. Pharmacol. 9, https://doi.org/10.3389/fphar.2018.00288 (2018).
Rippon, J. W. Medical Mycology: The Pathogenic Fungi and the Pathogenic Actinomycetes. 3rd edn (Saunders, Philadelphia, 1988).
Eliskases-Lechner, F., Guéguen, M. & Panoff, J. M. In Fuquay, J. W. (ed.) Encyclopedia of Dairy Sciences Vol. 102, 765–771 (Elsevier, 2011).
Pottier, I., Gente, S., Vernoux, J.-P. & Guéguen, M. Safety assessment of dairy microorganisms: Geotrichum candidum. Int. J. Food Microbiol. 126, 327–332 (2008).
pubmed: 17869364
doi: 10.1016/j.ijfoodmicro.2007.08.021
Bass, D. et al. Phylogeny and classification of Cercomonadida (Protozoa, Cercozoa): Cercomonas, Eocercomonas, Paracercomonas, and Cavernomonas gen. nov. Protist 160, 483–521 (2009).
pubmed: 19589724
doi: 10.1016/j.protis.2009.01.004
Massano, J. & Bhatia, K. P. Clinical approach to Parkinson’s disease: features, diagnosis, and principles of management. Cold Spring Harb. Perspect. Med. 2, a008870 (2012).
pubmed: 22675666
pmcid: 3367535
doi: 10.1101/cshperspect.a008870
Hantschel, J. et al. Effect of endometriosis on the fecal bacteriota composition of mice during the acute phase of lesion formation. PLoS ONE 14, e0226835 (2019).
pubmed: 31887116
pmcid: 6936831
doi: 10.1371/journal.pone.0226835
Bolyen, E. et al. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat. Biotechnol. 37, 852–857 (2019).
pubmed: 31341288
pmcid: 7015180
doi: 10.1038/s41587-019-0209-9
Pruesse, E. et al. SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res. 35, 7188–7196 (2007).
pubmed: 17947321
pmcid: 2175337
doi: 10.1093/nar/gkm864
McMurdie, P. J. & Holmes, S. phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS ONE 8, e61217 (2013).
pubmed: 23630581
pmcid: 3632530
doi: 10.1371/journal.pone.0061217
Hothorn, T., Hornik, K., van de Wiel, Mark, A. & Zeileis, A. A Lego system for conditional inference. Am. Stat. 60, 257–263 (2006).
doi: 10.1198/000313006X118430
Mandal, S. et al. Analysis of composition of microbiomes: a novel method for studying microbial composition. Microb. Ecol. Health Dis. 26, 27663 (2015).
pubmed: 26028277
Benjamini, Y. & Hochberg, Y. Controlling the false discovery rate−a practical and powerful approach to multiple testing. J. R. Stat. Soc. Ser. A Method 57, 289–300 (1995).
Best, D. J. & Roberts, D. E. Algorithm AS 89: the upper tail probabilities of Spearman’s Rho. Appl. Stat. 24, 377 (1975).
doi: 10.2307/2347111